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Expression in this Nucleus during Different Stress Conditions in Female Rats
Graduate School of Bioagricultural Sciences (M.A.C.E., H.T., B.A.S.R., Y.U., K.-I.M.), Nagoya University, Nagoya 464-8601, Japan; and Department of Biology (H.I.), Washington and Lee University, Lexington, Virginia 24450
Address all correspondence and requests for reprints to: Kei-ichiro Maeda, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan. E-mail: keimaeda{at}agr.nagoya-u.ac.jp.
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Abstract |
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(ER) expression in this nucleus during conditions of 48-h fasting, 2-deoxy-D-glucose (2DG)-induced acute glucoprivation and 1-h immobilization, in ovariectomized rats. Our approach was to examine the effect of lesioning catecholaminergic inputs to the PVN using DSAP [saporin-conjugated anti-DBH (dopamine-ß-hydroxylase)]. Bilateral injection of DSAP into the PVN, 2 wk before stress, prevented fasting-, glucoprivation-, and immobilization-induced increase in ER-immunopositive cells in the PVN. The DBH-immunoreactive (ir) terminals in the PVN were severely depleted by DSAP injection in all experimental groups. Among the brainstem noradreneregic cell groups examined, DBH-ir cell bodies were significantly reduced in the A2 region of all experimental groups treated with DSAP compared with the saporin- and vehicle-injected controls. PVN DSAP injection caused a small, but not significant, decrease in A1 DBH-ir cell bodies in fasted and immobilized rats, and a significant, but slight, reduction in A1 DBH-ir cell bodies of iv 2DG- injected rats compared with PVN vehicle-injected or PVN saporin-injected controls. The A6 DBH-ir cell bodies in all experimental groups treated with DSAP, saporin, or vehicle did not show any significant difference. These results suggest that the brainstem catecholaminergic inputs to the PVN, especially from the A2 cell group, may play a major role in mediating the induction of ER expression in the PVN by metabolic stressors such as fasting, acute glucoprivation, and less specific stressors, such as immobilization, in female rats. |
Introduction |
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-methyl-p-tyrosine into the PVN prevents the inhibitory effect of fasting (9) or acute glucoprivation (6) on LH release, suggesting a critical role for NE released in the PVN in LH suppression during metabolic stress. Furthermore, intracerebroventricular (icv) injection of 2-noradrenergic receptor antagonist reverses fasting-induced suppression of LH secretion (10), and immobilization-induced suppression of LH secretion is prevented by icv injection of either 1- or 2-noradrenergic receptor antagonists (8). Acute 2DG-induced glucoprivation stimulates c-fos expression in noradrenergic neurons in the lower brainstem (11). Lesioning of these brainstem noradrenergic neurons prevented the acute 2DG-induced increase in fos expression in the PVN in male rats (12) and chronic 2DG-induced suppression of estrous cyclicity in female rats (13). Taken together, these data suggest that brainstem noradrenergic inputs to the PVN are parts of the neural circuitry mediating suppression of reproductive functions during fasting, acute and chronic glucoprivation, and immobilization in female rats.
Several reports show that the noradrenergic neurons also regulate estrogen receptor (ER) expression in the rat hypothalamus (14, 15). Inhibition of NE release by administration of dopamine-ß-hydroxylase (DBH) inhibitors (14) or of NE action by 1- and 2-noradrenergic receptor antagonists (15) results in a decrease in hypothalamic ER. An increase in ER-containing cells in the PVN and A2 region of the nucleus of the solitary tract (NTS) has been demonstrated in response to fasting and immobilization stress (16). Similarly, glucoprivation induces an increase in ER expression in the PVN, and A2 and A1 regions of the brainstem (17). The increase in ER expression in these brain areas appears to be important for estrogen to potentiate fasting- (18) and acute glucoprivation- (19) induced suppression of LH secretion in female rats. In this context, the PVN and A2 region were identified as estrogen feedback sites for fasting-induced suppression of pulsatile LH secretion (20). Based on the preceding results, we hypothesize that brainstem noradrenergic inputs to the PVN may also mediate the induction of ER expression in the PVN during metabolic stress, such as fasting, acute glucoprivation, as well as during less specific stress of immobilization.
In the present study, we examined whether targeted lesioning of noradrenergic inputs to the PVN by local injection of an immunotoxin, saporin-conjugated anti-DBH (DSAP), into the PVN would prevent the increase in the number of ER-immunoreactive (ER-ir) cells in the PVN during fasting, glucoprivation and immobilization. DSAP is a specific catecholaminergic immunotoxin that is selectively taken up by catecholaminergic neurons (21, 22) and retrogradely transported back to the catecholaminergic cell bodies (23), where saporin destroys the catecholaminergic neuron by inactivation of the ribosomes (24). In addition, we determined the brainstem catecholaminergic cell group involved in regulating ER expression in the PVN in the above-mentioned conditions.
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Materials and Methods |
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We used ovariectomized (OVX) rats to negate estrogen modulation of ER expression (25). The ER antibody used in the present study has been reported to recognize both occupied and unoccupied receptors (26).
The present study was approved by the Committee on Animal Experiments of the Graduate School of Bioagricultural Sciences, Nagoya University.
Brain surgery
One week after ovariectomy, a stainless-steel guide cannula (26 gauge, Plastics One Inc., Wallingford, CT) was stereotaxically implanted into the PVN. The tip of the cannula was placed at 2.3 mm posterior, 7.5 mm ventral, and 0.6 mm lateral to the bregma. DSAP (totally 20 ng in 400 nl artificial cerebrospinal fluid (aCSF) per head; Advanced Targeting Systems, San Diego, CA) was bilaterally injected into the PVN (200 nl solution/side) through an internal cannula (31 gauge, Plastics One Inc.) for 2 min with a microinjection pump (EP-60, EICOM, Kyoto, Japan). The cannula was left in place for another 2 min for adequate diffusion of the toxin before withdrawal. The dose of DSAP was reported to be effective in destroying catecholaminergic neurons when given icv or directly into a specific brain area (21, 22). Control rats were infused bilaterally with vehicle (200 nl aCSF) or unconjugated saporin (4.2 ng in 400 nl aCSF; Advanced Targeting Systems). The amount of unconjugated saporin was determined to be the same amount of saporin present in the DSAP as stated in the manufacturer’s product information. The infusion flow rate was 100 nl/min using a microinjection pump.
Experimental protocols
A 2-wk recovery was allowed after brain surgery because significant noradrenergic cell loss has been observed in specific brain regions 14 d after central administration of DSAP (21, 22). The animals were then subjected to fasting, acute 2DG-induced glucoprivation or immobilization.
PVN vehicle- (n = 6), DSAP- (n = 4), or saporin- (n = 6) injected rats were subjected to 48-h fasting starting at 1300 h and then perfused immediately after the end of the fasting period and prepared for immunohistochemistry. Water was available ad libitum throughout the experimental period. An additional PVN vehicle-injected group of ad libitum-fed rats (n = 5) with free access to food and water were perfused and prepared for immunohistochemistry.
PVN vehicle- (n = 6), DSAP- (n = 4), or saporin- (n = 6) injected rats were iv injected with 2DG (200 mg/kg body weight) via an atrial cannula which was inserted on the previous day. This dose of 2DG suppresses pulsatile LH secretion in estradiol-treated OVX rats but not in OVX rats (19), and increases ER-containing cells in the PVN, and A1 and A2 regions of the brainstem in OVX rats (17). In addition, a group of vehicle-injected rats (n = 4) was iv injected with xylose (200 mg/kg body weight) through an atrial cannula. One hour after 2DG or xylose injection, rats were killed and prepared for immunohistochemistry.
PVN vehicle- (n = 6) or DSAP- (n = 6) injected rats were subjected to 1-h immobilization. Animals were then immediately perfused and prepared for immunohistochemistry. A corresponding vehicle-injected group (n = 5) was kept quietly inside the cage with free access to food and water and then perfused and prepared for immunohistochemistry.
Perfusion and immunohistochemistry
Rats were deeply anesthetized with sodium pentobarbital (40–50 mg/kg) at the end of each treatment and perfused with 4% paraformaldehyde in phosphate buffer as described previously (16). The brain was immediately removed from the skull, postfixed with the same fixative for 2–3 h at 4 C, and then cryoprotected with 30% sucrose in 0.05 M phosphate buffer for 2–3 d at 4 C. Serial coronal sections (50 µm in thickness) containing the PVN, and A1, A2, and A6 regions were obtained using a cryostat and then stored at –20 C in a cryoprotectant. Every fourth section through the PVN from each rat was processed for ER immunohistochemistry with the avidin biotin complex method (Vectastain Elite kit, Vector Laboratories, Burlingame, CA) that has been previously described (16). Tissue sections were incubated in AS-409 antirat ER serum (1:20,000) for 7 d at 4 C. ER-immunoreactivities were visualized by reaction with 0.05% 3'3-diaminobenzidine and 0.05% hydrogen peroxide in Tris buffer solution. Nuclear ER-immunoreactivities were examined under a light microscope. Tissue sections from the animals with various treatments and corresponding controls were processed simultaneously for immunohistochemistry. Each batch of sections includes sections containing the arcuate and ventromedial nuclei as positive controls for the ER immunohistochemistry.
To examine the extent of DSAP-induced lesioning of noradrenergic axon terminals and cell bodies, DBH immunostaining of every fourth section through the PVN and every third section through the A1, A2, and A6 brainstem regions was performed using a previously validated protocol (27). Tissue sections from each rat were incubated in mouse anti-DBH antibody (1:2000; Chemicon International Inc., Temecula, CA) for 3 d at 4 C, followed by incubation in biotinylated horse antimouse IgG (Chemicon) for 90 min and avidin biotin complex for 60 min. DBH immunoreactivities were visualized using 3'3-diaminobenzidine as chromogen.
The A1, A2, and A6 brainstem regions were specifically examined because it is well documented that noradrenergic fibers from these regions terminate in the PVN, and thus supply the noradrenergic innervation to this nucleus (1, 28). Furthermore, our previous findings showed a significant number of A1 and/or A2 DBH neurons colocalized with ER during 2DG-induced glucoprivation and fasting (17, 27), suggesting the involvement of A1 and A2 noradrenergic neurons in the neural circuitry of estrogen potentiation of metabolic stress-induced suppression of LH secretion in female rats.
Data analysis
The hypothalamic and brainstem areas examined in the present study were identified based on the previous work by Swanson and Kuypress (29) and brain atlas of Paxinos and Watson (30). Slides were coded to prevent bias while conducting cell count analysis. ER-ir cells in the subnuclei of the parvocellular PVN namely the anterior (PVHap), medial (PVHmp), dorsal (PVHdp), lateral (PVHlp), and periventricular (PVHpv) and DBH-ir cells in the A1, A2, and A6 regions were counted bilaterally at the following anatomical levels (mm caudal to the bregma): PVN (2.12–0.80 mm); A1 (14.60–13.68 mm); A2 (14.60–13.68 mm); A6 (10.52–9.16 mm). ER-ir cells were only counted in the parvocellular PVN because our previous studies show that this is the area in the PVN where ER-ir cells are found during the different stress conditions of fasting, acute 2DG-induced glucoprivation and immobilization (16, 17). Every fourth section through the PVN and every third section through A1, A2, and A6 brainstem region sections were used for quantification. Counts were performed twice, and the average was calculated. DBH-ir terminals in the PVN were examined, but quantification was not performed because of the difficulty in achieving an accurate count.
Significant differences between groups were determined by ANOVA followed by the Newman-Keuls post hoc test. Values were considered significant when P < 0.05.
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Results |
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shows schematic drawings of the cannula placements of all individuals in each group. Most of animals appear to have a similar site of PVN injection located at or just above the dorsal parvocellular PVN, regardless of treatments.
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-immunoreactivities in the PVN shows ER-immunoreactivities in the parvocellular PVN of representative vehicle-, DSAP-, and saporin-injected rats followed by fasting, acute 2DG-induced glucoprivation, immobilization or control conditions. Mean results of the number of ER-ir cells in each group are shown in Fig. 3.
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-ir cells throughout the PVN (Figs. 2A
and 3). Likewise, there were few ER-ir cells throughout the PVN in PVN vehicle-injected rats with iv xylose or without immobilization (Figs. 2, E and I, and 3). On the other hand, 48-h fasting (Fig. 2, B and D), acute 2DG-induced glucoprivation (Fig. 2, F and H) or immobilization (Fig. 2J) caused a marked increase in the number of ER-ir cells in the parvocellular PVN of PVN vehicle- or saporin-injected rats (Fig. 3). Specifically, a significant (P < 0.05) increase in ER-ir cells was observed in the medial parvocellular PVN in fasted and immobilized rats with vehicle or saporin injection in the PVN compared with corresponding controls (Fig. 3). In 2DG-treated rats that received vehicle or saporin injection into the PVN, significant (P < 0.05) increase in ER-ir cells were found not only in the medial, but also in the dorsal and lateral parvocellular PVN (Figs. 2, F and H, and 3). DSAP injection blocked the stimulatory effect of fasting (Fig. 2C), acute 2DG-induced glucoprivation (Fig. 2G) or immobilization (Fig. 2K) on ER expression in each subnucleus of the parvocellular PVN (Fig. 3).
DBH-immunoreactivities in the PVN and A2, A1, and A6 regions
Figure 4 shows DBH immunoreactivity in the PVN of representative PVN vehicle-, DSAP-, and saporin-injected rats after fasting, acute 2DG-induced glucoprivation, immobilization, or control conditions. PVN vehicle-injected rats fed ad libitum (Fig. 4A) or fasted (Fig. 4B) showed numerous DBH-ir terminals in the PVN. PVN DSAP injection resulted in a marked depletion of DBH-ir terminals in the PVN of fasted rats with some fibers spared mostly in the periventricular parvocellular and magnocellular PVN (Fig. 4C, inset), whereas unconjugated saporin injection into the PVN did not affect DBH-ir terminals in this nucleus of such rats (Fig. 4D). Many PVN DBH-ir terminals were found in PVN vehicle-injected rats treated with iv xylose or 2DG (Fig. 4, E and F). In 2DG-treated rats, PVN DSAP injection, but not saporin injection, caused a marked reduction in PVN DBH-ir terminals (Fig. 4, G and H). Dense DBH-ir terminals were also observed in PVN vehicle-injected nonimmobilized (Fig. 4I) and immobilized (Fig. 4J) rats. DSAP injection into the PVN caused a decrease in DBH-ir terminals in immobilized rats (Fig. 4K). In the 2DG-treated or immobilized animals, some fibers were also spared in the periventricular parvocellular and magnocellular PVN. Thus, PVN DSAP injection caused an apparent decrease in DBH-ir terminals within the PVN of all DSAP-injected rats compared with vehicle- or saporin-injected rats regardless of treatment conditions.
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indicates DBH immunoreactivities in the A1, A2, and A6 brainstem regions of representative vehicle-, DSAP-, and saporin-injected rats after 48-h fasting. Mean results of the number of DBH-ir cells in fasted, 2DG-injected or immobilized group are shown in Fig. 6
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and 6) and xylose-treated (Fig. 6). PVN injection of DSAP, saporin or vehicle in fasted (Figs. 5, B–D, and 6) rats did not significantly affect the A1 DBH-ir cells. In acute 2DG-treated rats, PVN DSAP injection caused a significant but slight decrease in A1 DBH-ir cell bodies compared with the PVN vehicle or saporin injection (Fig. 6). PVN DSAP injection in immobilized rats caused a slight, but nonsignificant decrease in A1 DBH-ir cell bodies when compared with PVN vehicle-injected rats with or without immobilization (Fig. 6). Thus, PVN DSAP injection tended to decrease the number of A1 DBH-ir cell bodies, although a decline was significant only in acute 2DG-treated rats (Fig. 6).
In the A2 region, numerous DBH-ir cell bodies were observed in PVN vehicle-injected rats fed ad libitum or fasted (Fig. 5, E and F). Statistical analysis (Fig. 6) showed that DSAP injection into the PVN caused a marked decrease in the number of A2 DBH-ir cell bodies in 48-h fasted rats (Fig. 5G) compared with those animals with vehicle (Fig. 5F) or saporin (Fig. 5H) injection into the PVN. Similar results were obtained in acute 2DG-treated and immobilized groups (Fig. 6, immunohistochemical data not shown). Thus, PVN DSAP injection significantly decreased the number of DBH-ir cell bodies in the A2 brainstem region of all DSAP-injected rats compared with vehicle- or saporin-injected rats regardless of treatment conditions (Fig. 6).
Numerous DBH-ir cell bodies and processes were found in the A6 region of PVN vehicle-, saporin- and DSAP-injected rats (Fig. 5, I–L). PVN DSAP injection did not have any significant effect on the number of A6 DBH-ir cell bodies compared with vehicle- or saporin-treated controls regardless of the treatment conditions (Fig. 6).
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Discussion |
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-ir cells in the PVN of OVX rats. Because DSAP administration into the PVN caused a marked loss of PVN DBH-ir terminals in all experimental groups, catecholaminergic inputs to the PVN may mediate the induction of ER in the PVN induced by these metabolic and less specific stressors, i.e. fasting, acute glucoprivation, and immobilization, in the rat. This is consistent with previous studies showing that NE release and turnover rate in the PVN are increased by fasting, acute glucoprivation, and immobilization in rats (5, 6, 7), and noradrenergic neurons stimulate ER expression in the rat hypothalamus (14, 15).
In the present study, the number of A2 DBH-ir neurons markedly declined after PVN DSAP injection in fasted, 2DG-injected, and immobilized rats. This significant reduction of A2 DBH-ir neurons by 88–90% and almost complete loss of DBH-ir axon terminals in the PVN after DSAP injection, together with decreased ER expression in the PVN, suggest that the A2 catecholaminergic input to the PVN plays a major role in stimulating ER expression in the PVN during these different stress conditions. The number of A1 DBH-ir neurons in both fasted and immobilized rats was not significantly but only slightly decreased by DSAP injection, whereas the PVN DSAP injection in acutely glucoprivic rats significantly reduced the A1 DBH-ir neurons. These results suggest that an additional population of catecholaminergic neurons in the A1 region might contribute to ER induction under stressful conditions. The A6 DBH-ir neurons were generally spared after PVN DSAP injection in all experimental groups, suggesting that this brainstem catecholaminergic cell group is not involved in the induction of ER expression in the PVN by fasting, acute glucoprivation, or immobilization stress in female rats. The present findings are consistent with previous anatomical observations. The PVN is densely innervated by noradrenergic axon terminals originating mainly from the A2 region and partly from A1 and A6 brainstem noradrenergic cell groups (1, 28). The A2 and A1 cell groups provide 70% and 20% of the noradrenergic afferents to the PVN, respectively (1, 28, 31). The A2 cell group terminates to the dorsal and medial parvocellular PVN, whereas the A1 cell group terminates to both parvocellular and magnocellular PVN with majority of the fibers projecting to the latter region (1, 28). The majority of A6 noradrenergic neurons particularly terminate to the periventricular PVN (1, 28). These reports are consistent with the present results showing that ER-ir cells are exclusively distributed in the medial parvocellular PVN of rats with any of the stresses and additionally in the dorsal and lateral parvocellular PVN of rats with acute glucoprivation (16, 17).
The marked loss of catecholaminergic innervation to the PVN in PVN DSAP-injected rats is consistent with the results of Ritter et al. (12) and I’Anson et al. (13). A decrease in catecholaminergic cell bodies was also found in the A1 and A2 regions of the brainstem in these latter studies. We found a similar significant decrease in catecholaminergic cell bodies in the A2 region of the brainstem. However, the reduction in the cell bodies in the A1 region of the brainstem was minimal and only reached significance in PVN DSAP-injected rats subjected to acute glucoprivation. Our present results also show that PVN DSAP injection did not significantly reduce the A6 catecholaminergic cell bodies, whereas Ritter et al. (12) observed a marked decrease in the number of tyrosine hydroxylase-ir cells in the A6 region of the brainstem. First, the difference between our study and the two earlier studies may be attributed to slight difference in PVN injection site (Ref.12 , within the parvocellular PVN) or a different dose of DSAP (12, 13). The present study used a lower dose less than half compared with two earlier studies (12, 13), which may cause a smaller area of DSAP diffusion in more dorsal part of the PVN. The difference between ours and earlier studies may also be due to the use of a different sex and strain of the rat (13), different steroid milieu, or immunohistochemistry (Ref.12 , used tyrosine hydroxylase immunostaining).
The A2 region of the NTS is a major relay center of sensory information from the peripheral system to the forebrain via the vagus nerve (32, 33). In addition, the PVN and A2 region appear to be estrogen feedback sites for fasting-induced suppression of pulsatile LH secretion (20). These vagal afferent fibers form synapses with A2 DBH-ir cells, indicating that A2 noradrenergic neurons receive direct synaptic inputs from sensory vagal afferents (34). Our previous results demonstrate that transection of the vagal trunks prevented fasting-induced increase in ER expression in the A2 region and PVN of OVX rats (35). Taken together with our new findings, we hypothesize that, during fasting, sensory signals are transmitted by the vagus nerve from the upper digestive tract to induce ER expression in the A2 noradrenergic neurons, resulting in an increase in ER in the PVN.
Unlike fasting where the signal is sensed peripherally (36), a glucoprivic signal seems to be detected centrally (37). This is supported by previous findings wherein total subdiaphragmatic vagotomy failed to prevent a 2DG-induced increase in food intake (38), whereas lesions of the lower brainstem nuclei, NTS and area postrema abolished the 2DG-induced increase in food intake (38) and suppression of estrous cyclicity (39). Moreover, 2DG treatment activates lower brainstem neurons including the A1 and A2 catecholaminergic neurons (3, 40, 41). These A1 and A2 catecholaminergic neurons were also observed to possess a majority of the ER in 2DG-treated rats (17), implying that glucoprivic signals detected by the lower brainstem induce ER expression in A1 and A2 catecholaminergic neurons, which then stimulate the induction of ER in the dorsal and lateral parvocellular PVN (Fig. 3B), in addition to the medial parvocellular PVN. Most recently, I’Anson et al. (13) showed that ascending noradrenergic pathways from A1 and A2 brainstem regions transmit the glucoprivic signal to the reproductive axis via the PVN in cycling female rats. Thus, it is likely that induction of ER expression in A1 and A2 catecholaminergic neurons potentates the glucoprivic signal to the reproductive axis via the same pathways.
Immobilization stress has been suggested to activate catecholaminergic neurons from the A1, A2, and A6 regions (2), whereas in the present study induction of ER expression in the PVN appears to be primarily mediated by the A2 catecholaminergic neurons. The activation of these brainstem catecholaminergic inputs to the PVN may mediate immobilization-induced suppression of LH secretion (42), but the role of PVN ER increase in the suppression is unclear.
In summary, the present results demonstrate that the brainstem catecholaminergic inputs to the PVN, especially from the A2 cell group, play a major role in ER expression in the PVN in response to fasting, acute 2DG-induced glucoprivation and immobilization. This catecholaminergic stimulation of ER expression in the PVN during fasting and acute glucoprivation may be important for estrogen enhancement of LH suppression, and thus reproductive axis suppression, in female rats. The expression of ER in the PVN during less specific stress, such as immobilization, is also mediated by catecholaminergic inputs to the PVN, and suggests a similar transduction pathway for less specific stressors in the suppression of the female reproductive axis.
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Acknowledgments |
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antibody and Ms. Y. Niwa and K. Arakawa of Nagoya University for the technical assistance. |
Footnotes |
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Abbreviations: aCSF, Artificial cerebrospinal fluid; DBH, dopamine-ß-hydroxylase; 2DG, 2-deoxy-D-glucose; DSAP, saporin-conjugated anti-DBH; ER, estrogen receptor; icv, intracerebroventricular; ir, immunoreactive; NE, norepinephrine; NTS, nucleus of the solitary tract; OVX, ovariectomized; PVN, paraventricular nucleus.
Received April 13, 2004.
Accepted for publication July 12, 2004.
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References |
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2-adrenergic receptors are involved in the suppression of luteinizing hormone release during acute fasting in the ovariectomized estradiol-primed rats. Neuroendocrinology 56:724–728[Medline]
2-noradrenergic receptors. Brain Res 404:51–57[CrossRef][Medline]
immunoreactivity in the brain catecholaminergic neurons in ovariectomized rats. Neurosci Lett 299:109–112[CrossRef][Medline]
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